Neuroanatomical differences in visual, motor, and language cortices between congenitally deaf signers, hearing signers, and hearing non-signers

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ORIGINAL RESEARCH ARTICLEpublished: 02 August 2013

doi: 10.3389/fnana.2013.00026

Neuroanatomical differences in visual, motor, andlanguage cortices between congenitally deaf signers,hearing signers, and hearing non-signersJohn S. Allen1,2, Karen Emmorey3*, Joel Bruss4 and Hanna Damasio1,2

1 Dornsife Cognitive Neuroscience Imaging Center, University of Southern California, Los Angeles, CA, USA2 Brain and Creativity Institute, University of Southern California, Los Angeles, CA, USA3 Laboratory for Language and Cognitive Neuroscience, San Diego State University, San Diego, CA, USA4 Laboratory of Computational Neuroimaging, Department of Neurology, University of Iowa Carver College of Medicine, Iowa City, IA, USA

Edited by:

Alfonso Fairén, University MiguelHernandez, Spain

Reviewed by:

Gundela Meyer, Universidad de LaLaguna, SpainKathleen S. Rockland, BostonUniversity School Medicine, USA

*Correspondence:

Karen Emmorey, Laboratory forLanguage and CognitiveNeuroscience, San Diego StateUniversity, 6495 Alvarado Road,Suite 200, San Diego, CA 92120,USAe-mail: [email protected]

We investigated effects of sign language use and auditory deprivation from birth on thevolumes of three cortical regions of the human brain: the visual cortex surrounding thecalcarine sulcus in the occipital lobe; the language-related cortex in the inferior frontal gyrus(pars triangularis and pars opercularis); and the motor hand region in the precentral gyrus.The study included 25 congenitally deaf participants and 41 hearing participants (of which16 were native sign language users); all were right-handed. Deaf participants exhibited alarger calcarine volume than hearing participants, which we interpret as the likely result ofcross-modal compensation and/or dynamic interactions within sensory neural networks.Deaf participants also had increased volumes of the pars triangularis bilaterally comparedto hearing signers and non-signers, which we interpret is related to the increased linguisticdemands of speech processing and/or text reading for deaf individuals. Finally, althoughno statistically significant differences were found in the motor hand region for any of thegroups, the deaf group was leftward asymmetric, the hearing signers essentially symmetricand the hearing non-signers were rightward asymmetric – results we interpret as thepossible result of activity-dependent change due to life-long signing. The brain differenceswe observed in visual, motor, and language-related areas in adult deaf native signersprovide evidence for the plasticity available for cognitive adaptation to varied environmentsduring development.

Keywords: deaf, sign language, inferior frontal gyrus, motor hand region, calcarine, morphometry

INTRODUCTIONAcross the lifespan, the structural and functional plasticity ofthe mammalian brain is expressed through a variety of mech-anisms and pathways. Several factors influence the potentialplastic response of the brain to environmental influences. Theextreme and inherent plasticity of the brain in early develop-ment is “braked” by a variety of cellular processes that serveultimately to demarcate a critical or sensitive learning period,during which highly stable functional pathways are trained andestablished (Bavelier et al., 2010). Cortical plasticity is expressedin numerous brain regions, including both motor and sensorypathways (Dunlop, 2008; Fu and Zuo, 2011). Brain changesassociated with various forms of skill learning have been inves-tigated to address questions of brain plasticity. For example,multiple changes in brain structure and function have beendetected in musicians compared to non-musicians (Gaser andSchlaug, 2003; Wan and Schlaug, 2010). Another way brain plas-ticity has been investigated is by studying individuals whosesensory experiences or cognitive demands, often beginning inchildhood, are profoundly different from normal experience.For example, blind individuals show changes in brain anatomythat correlate with the length of time blindness has beenexperienced, with early-onset blind individuals showing more

pronounced changes than late-onset individuals (Noppeney, 2007;Leporé et al., 2010a).

A potentially valuable source of insights into the structuraland functional plasticity of the human brain is the neurocog-nitive study of deaf and hearing individuals who are nativeusers of a sign language (MacSweeney et al., 2008; Emmorey andMcCullough, 2009). Congenitally deaf signers are particularlyinteresting for the study of brain plasticity because changes intheir structural neuroanatomy could reflect the effects of bothskill learning (i.e., the acquisition of a signed language) andsensory deprivation. Given the intense long-term visual andmanual experiences associated with learning a sign languagefrom birth, both deaf and hearing signers may be expected toprovide evidence of plasticity associated with learning a demand-ing cognitive and motor skill. Indeed, this prediction has beensupported by functional neuroimaging studies. Sign languageproduction activates many of the same areas of the brain asspoken language, but the additional activation of the left pari-etal lobe in sign language production provides evidence of thebrain’s capacity for functional plasticity in response to noveldemands (Emmorey et al., 2007; MacSweeney et al., 2008). Struc-tural differences in the insula have also been documented in bothhearing and deaf signers, compared to non-signers and have been

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interpreted as a result of sign language expertise (Allen et al.,2008a).

Due to auditory deprivation during critical developmentalperiods, some neural changes should be evident in deaf com-pared to hearing individuals. Auditory regions of the brain are anobvious candidate for plastic changes, and we have shown thatdeaf people have decreased white matter in and around Heschl’sgyrus, the anatomical landmark for the primary auditory cortex(Emmorey et al., 2003); this finding was later replicated by Shibata(2007). This difference presumably arises as a result of decreasedlevels of connectivity within, into, and out of the primary auditorycortex, even if this region is co-opted for other functions in deafindividuals (Bavelier and Hirshorn, 2010). We have also shownthat deaf individuals have an increased volume in the cortex ofthe posterior insula, which is not present in hearing signers (Allenet al., 2008a). The increased volume of the posterior insula maybe related to the dependence of deaf individuals on lip reading forspeech comprehension; functional neuroimaging has shown thatdeaf, but not hearing, individuals activate the insula during speechreading (MacSweeney et al., 2001).

Here we investigate the effects of sensory deprivation and signlanguage expertise on plasticity in the human brain by comparingregional cortical volumes in adult, right-handed congenitally deafsigners, hearing signers who acquired American Sign Language(ASL) from birth from their deaf families, and hearing non-signers. We used high-resolution magnetic resonance imaging(MRI) and anatomical landmark-based morphometry to directlymeasure the cortical volumes of three important and informa-tive regions incorporating visual, language, and motor areas: (1) aprimary sensory cortical region – the cortex surrounding the cal-carine sulcus in the medial occipital lobe, a proxy for the primaryvisual cortex or Brodmann area (BA) 17 (Amunts et al., 2000);(2) an association cortex region important for language – Broca’sarea within the left inferior frontal gyrus (IFG), and its righthemisphere homolog, subdivided into pars opercularis and parstriangularis (Keller et al., 2007); and (3) a primary motor region –the motor-hand cortex, or handknob, located within the precen-tral gyrus (Yousry et al., 1997). For each of these three regions,automated volumetry/densitometry research on deaf individualshas indicated that structural differences may arise as a result ofauditory deprivation or sign language experience (Penhune et al.,2003; Leporé et al., 2010b; Pénicaud et al., 2012). We look to con-firm and expand upon these results using a region of interest(ROI) approach with manually delineated regions and volumecalculations performed on individual subjects.

Based on previous studies of enhanced visual ability in deafindividuals (for recent reviews, see Bavelier et al., 2006; Pavaniand Bottari, 2012), we predicted that the calcarine cortex volumeshould show a difference between the deaf group and the twohearing groups in accordance with such altered visual ability. Bot-tari et al. (2010, 2011) have recently shown that congenitally deafadults exhibit enhanced “visual reactivity” (superior performanceon speeded visual detection tasks), which was associated with veryearly event-related potential (ERP) changes in striate cortex. Theseneurobehavioral changes might also co-occur with macroanatom-ical changes in striate cortex for the deaf group. Difference in graymatter volume for deaf native signers might also be linked to the

early age at which sign language acquisition took place; Pénicaudet al. (2012) recently reported that deaf late learners of a sign lan-guage exhibited reduced gray matter density in primary visualcortex.

Previous studies also suggest that frontal language regions maybe modified by sign language experience or deafness. In a tensor-based morphometry (TBM) study with 14 deaf native signers,Leporé et al. (2010b) found that white matter volumes in Broca’sarea and the right frontal operculum were significantly larger forthe deaf group compared to hearing non-signing controls. Func-tionally, Broca’s area and its right homolog have been shown to beinvolved in sign language comprehension (e.g., Neville et al., 1998;MacSweeney et al., 2002). In addition, functional neuroimagingstudies that examine phonological processing of speech and read-ing in deaf signers report greater activation in Broca’s area andits right hemisphere homolog compared to hearing non-signers(MacSweeney et al., 2009; Corina et al., 2012). Thus, it is cur-rently unclear whether sign language experience or deafness (andthe consequent changes in spoken language processing) influencesthe size of inferior frontal language-related cortices. The inclusionof hearing native signers in our study will help to tease apart thesetwo possibilities.

Finally, Penhune et al. (2003) conducted a voxel-based mor-phometry (VBM) study with a small group of deaf native signers(N = 12) and reported increased gray matter density in the leftmotor hand area compared to hearing non-signers. The authorshypothesized that increased fine motor control of the dominanthand during signing contributed to volume increases in this area.If this hypothesis is correct, then we should observe differencesin the size and/or asymmetry of the motor cortex in the handregion (the handknob) for the signing participants (both deaf andhearing) compared to the non-signers. However, changes in motorcortex may be even more pronounced for deaf signers because ASLis their dominant and most frequently used language compared tohearing signers (see Emmorey et al., 2013a).

In sum, we directly measured the cortical volumes of primaryvisual, language-related, and motor regions that may be affectedby the early acquisition and life-long use of a signed languageand/or by congenital deafness. The inclusion of a group of hearingnative signers allows us to tease apart effects of deafness from signlanguage-related effects.

MATERIALS AND METHODSPARTICIPANTSParticipants were 25 congenitally deaf individuals who were nativeASL signers (14 women and 11 men, average age = 23.8 years,SD = 4.1, range = 19–38), 25 hearing individuals with no knowl-edge of ASL (14 women and 11 men, average age = 28.5 years,SD = 4.5, range = 22–39), and 16 hearing individuals whoacquired ASL as young children from their deaf parents (10 womenand 6 men, average age = 24.3 years, SD = 4.4, range = 19–38).The hearing signers (who had no history of hearing loss) wereborn into deaf signing families and acquired expertise in ASL aschildren, concurrently with their acquisition of spoken language.The hearing non-signers were monolingual English speakers withno history of hearing loss. All subjects were right-handed, withscores on the Oldfield–Geschwind Handedness Inventory > +90

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(maximum right-handed score +100). All subjects were healthywith no history of neurological or psychiatric illness. Twenty-one deaf subjects exhibited profound hearing loss (>90 dB inthe better ear), three subjects had severe hearing loss (>75 dBin the better ear), and one subject had moderately severe hear-ing loss (>55 dB in the better ear). Data on early hearing aiduse was available for 17 deaf subjects. None used a hearing aidconsistently before the age of 2. Eleven were required to wear hear-ing aids at school, but only two also wore hearing aids at home,and six subjects did not wear hearing aids at home or at school.All deaf subjects were congenitally deaf and were born to deafparents, and ASL was their primary and first language. All sub-jects gave informed consent in accordance with institutional andfederal rules.

MR IMAGE ACQUISITION AND PROCESSINGBrain image data were collected as previously described (Emmoreyet al., 2003; Allen et al., 2008a). Thin cut MR images were obtainedin a GE Signa scanner operating at 1.5 T by using the followingprotocol: SPGR/50, TR 24, TE 7, NEX 1 matrix 256 × 192, field ofview (FOV) 24 cm. We obtained 124 contiguous coronal slices, 1.5or 1.6 mm thick and interpixel distance 0.94 mm. Three individual1NEX SPGR datasets were obtained for each subject during eachimaging session. These were coregistered and averaged post hocusing Automated Image Registration (AIR 3.03, UCLA; Woodset al., 1992; Holmes et al., 1998).

Magnetic resonance image analysis (3D reconstructions andvolume determinations from ROIs) were conducted using Brain-vox (Frank et al., 1997), an interactive family of programs designedto reconstruct, segment, and measure brains from MR acquiredimages. An automated program, extensively validated againsthuman experts, was used to segment the images into the threeprimary tissue types (white, gray, cerebral spinal fluid; Grabowskiet al., 2000). Although the ROIs may include white matter inthe tracings, only gray matter (cortical) volumes are reported.Before tracing ROIs, brains were realigned (but not resized;see Allen et al., 2008b for discussion) along a plane runningthrough the anterior and posterior commissures (i.e., the AC–PC line); this procedure ensured that coronal slices in all subjectswere perpendicular to a uniformly and anatomically defined axisof the brain.

REGIONS OF INTERESTRegions of interests were traced by hand in each hemisphere(by John S. Allen except for the handknob, see below) on con-tiguous coronal or axial slices of the brain. The study focusedon three cortical ROIs: the cortex surrounding the calcarinesulcus (corresponding to BA17), the pars triangularis and oper-cularis of the IFG (corresponding to BA45 and BA44, respec-tively and known as Broca’s area in the left hemisphere), andthe primary hand motor cortex (corresponding to a sector ofBA4) and clearly visible on axial and parasagittal MRI slices(Yousry et al., 1997). Total cerebral hemisphere gray matter vol-umes (excluding the basal ganglia) were determined as describedin Allen et al. (2003).

Following Brodmann’s demarcation of area 17 (primary visualcortex or striate cortex), both banks of the calcarine sulcus were

traced posterior to the intersection with the parieto-occipitalsulcus; anterior to this point, only the lower bank was traced(Figure 1A). The ROI of the calcarine cortex included all sidebranches until its termination at the occipital pole. The surfacecortex included was determined by extending a line from thecortical depth of the banks of the sulcus proper to the pial sur-face. It is important to note that while the calcarine sulcus is astrong anatomical landmark indicating the position of the pri-mary visual cortex, the striate cortex itself extends variably ontothe mesial surface of the occipital lobe surrounding the calcarinesulcus (Amunts et al., 2000; Hinds et al., 2008, 2009). The propor-tion of striate cortex found within the calcarine may only be on theorder of 60% (Stensaas et al., 1974; Rademacher et al., 1993); how-ever, both the depth of the calcarine sulcus and the surface area ofcalcarine cortex correlate to overall striate cortex volume (Gilis-sen and Zilles, 1996). Thus, the volume of the calcarine cortex isalso likely to be correlated with the overall volume of the primaryvisual cortex.

Tracing of Broca’s area and the homologous region in the righthemisphere (consisting of the pars triangularis and pars oper-cularis) was done following Keller et al. (2007). As illustrated inFigure 1B, the boundaries for the pars opercularis were (1) ante-riorly, the ascending branch of the Sylvian fissure (AscSF); (2)posteriorly, the inferior precentral sulcus (PreCS); (3) superiorly,the inferior frontal sulcus (IFS); and (4) inferiorly, the Sylvianfissure (SF). The ascending branch of the SF does not typicallyreach the IFS, therefore a line connecting the superior end of theascending branch of the SF to the IFS was drawn perpendicularto the AC–PC plane to close this boundary. When the IFS didnot reach the inferior PreCS, a direct line, parallel to the AC–PCplane, from the posterior end of the IFS was used to close thesuperior boundary. The boundaries for the pars triangularis were:(1) posteriorly, the anterior boundary of pars opercularis formedpredominantly by the ascending branch of the SF; (2) inferiorly,the horizontal branch of the SF (HzSF); and (3) antero-superiorly,the IFS, as it extends anteriorly and inferiorly toward the anteriorend of the HzSF. A line was drawn from this point to the antero-inferior end of the IFS to close off the anterior boundary. If theIFS was broken into two or more segments, connecting lines weredrawn to link the segments. The pars triangularis and opercularisROIs included all of the cortex located within the boundaries. Graymatter volumes for Broca’s area and its right hemisphere homologwere determined by summing the volumes of the pars opercularisand triangularis.

The primary hand motor region is located in the superior por-tion of the precentral gyrus of the frontal lobe (Figure 1C). It canbe identified anatomically in MRI by a sector of the precentralgyrus projecting into the central sulcus (the handknob), which isclearly visible in the axial plane; its position can also be seen in bothparasagittal and coronal slices (Yousry et al., 1997; Sastre-Janeret al., 1998; Boling et al., 1999). In the axial plane, the hand-knob has characteristic omega (single gyrus) and epsilon (doublegyrus) forms. The handknob was traced on contiguous axial cuts(1.0 mm thick), which were parallel to the AC–PC plane; its iden-tity and location were confirmed by observation of its hook-likeappearance in the sagittal plane. Tracing proceeded superiorly andinferiorly from the axial plane in which the omega or epsilon

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FIGURE 1 | (A) The calcarine sulcus. The calcarine sulcus cortex (red) ROIprojected to the mesial surface of the left hemisphere. Following Brodmann’sdemarcation of area 17, both banks were traced posterior to the intersectionof the calcarine sulcus and the parieto-occipital sulcus (blue) (coronal slice a),but only the lower bank of sulcus was traced anterior to this intersection(coronal slice b). (B) Broca’s area (left hemisphere) of the inferior frontal gyrusdivided into the pars triangularis (PTri, red) and pars opercularis (POp, blue).Regions of interest were defined and traced as described in Section“Materials and Methods,” following Keller et al. (2007). IFS, inferior frontal

sulcus (yellow); AscSF, ascending branch of the Sylvian fissure (coral); HzSF,horizontal branch of the Sylvian fissure (green); PreCS, precentral sulcus(white). (C) Tracing the motor handknob. (c) The position of the motorhandknob (blue) is projected to the surface of the precentral gyrus. Thecentral sulcus is indicated by the broken gold line. (d) An axial slicedemonstrating the two classic forms of the handknob: the epsilon form in theright hemisphere and the omega form in the left hemisphere. All volumetrictracing of the handknob was done on contiguous 1-mm axial slices. R, right;L, left.

shaped handknob was identified. The boundaries for the hand-knob were the central sulcus and a line linking the depths of itslimiting lateral and medial sulci. The handknob was traced inde-pendently by two investigators (John S. Allen and Joel Bruss), andthen a consensus tracing was chosen following review of the trac-ings by both investigators. Tracing of the handknob was done blindto participant group membership. In addition to the handknob,the entire precentral gyrus was also traced. On the lateral surface,its limits were the PreCS, central sulcus, and the SF. On the mesialsurface, the paracentral sulcus was followed as an extension of thesuperio-mesial portion of the PreCS, and a line was drawn (per-pendicular to the AC–PC plane) from the end of the paracentralsulcus to the cingulate sulcus to form the mesial anterior bound-ary. The posterior mesial boundary was formed by the ascendingbranch of the cingulate sulcus; a line linking the end of this sulcusto the end of the central sulcus on the mesial surface completed thisboundary.

DATA ANALYSISStatistical analyzes were performed using SPSS 19 for Windows(IBM SPSS, Armonk, NY, USA). For each ROI, main effects ofhemisphere (left, right) and group (deaf, hearing non-signers,hearing signers) were assessed using a 2 × 3 repeated measuresanalysis of variance (ANOVA) with total cerebral cortical (gray

matter) volume as the covariable. Post hoc univariate ANOVAswith total cerebral cortical volume as covariable were used tocompare group means (deaf vs. hearing non-signers, deaf vs.hearing signers, hearing signers vs. hearing non-signers). Hemi-spheric asymmetries were also examined with a conventionalasymmetry index (AI) {(L − R)/[(L + R)/2]}.

RESULTSVolumes of major brain regions are often correlated for size(Allen et al., 2002), therefore before undertaking group-wisecomparisons of regional brain volumes, it is important to exam-ine if overall brain size is an important covariable. Cerebralgray matter volume was not significantly different among thethree subject groups (F = 1.136; df = 2,63; p = 0.328);however, the average volume of the hearing signer group wassomewhat smaller (587cc, SD = 58.3) than the deaf group(618cc, SD = 56.8) and the hearing non-signer group (606cc,SD = 74.0). Therefore, group differences for each of the targetregions were assessed with total cortical hemisphere volume as acovariable.

CALCARINE SULCUS CORTEX VOLUMEThe mean volumes of the left and right calcarine sulcus cortexare presented in Table 1 and Figure 2. The 2 × 3 repeated

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Table 1 | Cortical volumes of the left, right, and total (L + R) calcarine

cortex.

Deaf

signers

Hearing

signers

Hearing

non-signers

L calcarine cortex 5022 (838) 4464 (697) 4475 (733)

R calcarine cortex 5701 (1013) 5276 (604) 5139 (947)

L + R calcarine cortex 10723 (1679) 9740 (1027) 9615 (1570)

Volumes in mm3; L, left; R, right; standard deviations are in parentheses.

measures ANOVA showed a significant main effect for hemisphere(F = 7.295; df = 1,62; p = 0.009). The volume of the calcarinecortex was strongly rightwardly asymmetric in all three groups.AI scores were −0.124 (SD = 0.120) for the hearing non-signers,−0.108 (SD = 0.166) for the deaf signers, and −0.161 (SD = 0.156)for the hearing signers. There were no significant differencesamong the groups for AI score. Within each group, pair-sampledt-tests showed that the right calcarine was significantly larger thanthe left (all ps ≤ 0.001). The interaction between hemisphere andparticipant group was not significant.

The 2 × 3 ANOVA also showed a significant effect of group(F = 3.241; df = 2,62; p = 0.046). Post hoc group-wise compar-isons showed that total calcarine volume was significantly largerin the deaf participants compared to hearing non-signing partici-pants (F = 5.251; df = 1,47; p = 0.026). There were no significantdifferences between the hearing signing and non-signing partici-pants. Examining each hemisphere separately, we found that thedeaf participants’ left calcarine volume was significantly largerthan for both the hearing non-signers (F = 5.412; df = 1,47;p = 0.024) and the hearing signers (F = 4.295; df = 1,38;p = 0.045). The right calcarine was also larger in the deaf groupcompared to the other two groups, but the differences were notsignificant.

FIGURE 2 | Calcarine sulcus cortex volume. Deaf individuals havesignificantly larger calcarine volume than hearing individuals(error bars: ±1 standard error; *p < 0.05).

PARS TRIANGULARIS AND OPERCULARISThe volumetric results for the pars triangularis and pars opercu-laris for the left and right hemispheres are presented in Figure 3and in Tables 2 and 3. For the pars opercularis, there wereno main effects for hemisphere or group, although the lat-ter approached statistical significance (F = 2.672; df = 2,62;p = 0.077). There was no interaction between hemisphere andparticipant group.

For the pars triangularis, there was no significant main effect ofhemisphere or interaction between participant group and hemi-sphere. However, there was a significant main effect of group(F = 6.627; df = 2,62; p = 0.002). Post hoc tests showed the parstriangularis volumes were significantly larger for the deaf signerscompared to the hearing non-signers for the combined volume(L + R; F = 11.662; df = 1,47; p = 0.001), for the left hemi-sphere volume (F = 4.824; df = 1,47; p = 0.033), and for the righthemisphere volume (F = 9.678; df = 1,47; p = 0.003). A similarpattern was seen comparing the deaf signers to the hearing signers,with the combined volume (L + R) difference reaching statisticalsignificance (F = 4.889; df = 1,38; p = 0.033). There were no sig-nificant differences between the hearing non-signers and hearingsigners in the pars triangularis volumes.

MOTOR HANDKNOB CORTEXMotor handknob cortical volume results by hemisphere are pre-sented in Figure 4 and Table 4. The 2 × 3 ANOVA showed nosignificant main effects of hemisphere or group, and no interac-tion. It is interesting to note, however, that the asymmetry indicesof the three groups did vary substantially. The deaf individualswere leftwardly asymmetric, with the left hemisphere handknobbeing about 11% larger than the right, while the hearing non-signers were rightwardly asymmetric to an even greater degree(about 14% larger on the right). The hearing signers had essen-tially symmetrical handknobs. Comparing the deaf signers to thehearing non-signers (leaving the hearing signers out of the model),

FIGURE 3 | Volumes of the pars opercularis and pars triangularis. Thepars triangularis is significantly larger in deaf compared to hearingindividuals (error bars: ±1 standard error; *p < 0.05; **p < 0.01).

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Table 2 | Cortical volumes of pars opercularis, pars triangularis, and

combined pars triangularis and opercularis.

Deaf

signers

Hearing

signers

Hearing

non-signers

L pars opercularis 5716 (2152) 4914 (1204) 5262 (1406)

R pars opercularis 5793 (1746) 4484 (1099) 4582 (1210)

L + R pars opercularis 11509 (3518) 9398 (469) 9844 (2258)

L pars triangularis 5811 (1590) 4809 (1330) 4801 (1514)

R pars triangularis 5886 (1463) 4928 (1552) 4705 (1099)

L+R pars triangularis 11698 (2271) 9736 (2015) 9506 (2252)

ANCOVA results for the effect of group (using hemisphere cortical volume as acovariable). Bonferroni-corrected t-tests were used for post hoc group-wise com-parisons.Volumes in mm3; L, left; R, right; standard deviations are in parentheses,*P ≤ 0.05; **P ≤ 0.01.

Table 3 | Asymmetry index scores for the pars opercularis and pars

triangularis.

Deaf signers Hearing signers Hearing

non-signers

Pars opercularis

asymmetry index

−0.0306 (0.2725) 0.0912 (0.2911) 0.1332 (0.2776)

Pars triangularis

asymmetry index

−0.0184 (0.3211) −0.0142 (0.4280) −0.0006 (0.2974)

Asymmetry index: {(L − R)/[(L + R)/2]}.

FIGURE 4 | Volumes of the left and right handknobs (error bars: ±1

standard error).

the AI score was significantly different between the two groups(F = 5.243; df = 1,47; p = 0.027).

DISCUSSIONThe results presented here expand our perspective on the scopeof structural cortical plasticity associated with congenital deafness

Table 4 | Motor handknob cortical volumes and asymmetry indexes.

Deaf

signers

Hearing

signers

Hearing

non-signers

Left hemisphere

handknob

822 (296) 871 (270) 730 (216)

Right hemisphere

handknob

733 (260) 868 (284) 858 (288)

Handknob asymmetry

index

0.115 (0.401) 0.014 (0.393) −0.139 (0.416)

Asymmetry index: {(L − R)/[(L + R)/2]}.All volumes in mm3; standard deviations are in parentheses.

and life-long signing. We found significant differences betweenthe deaf and hearing groups in the cortex of the calcarine sulcusand the pars triangularis, while the handknob results suggestedthat this region may be lateralized differently in deaf signers com-pared to hearing non-signers. In general, the hearing signers weremore similar to the hearing non-signers than to the deaf signers,suggesting a primary influence of auditory deprivation in shapingneuroanatomical plasticity. This is not to say that the differencesobserved between deaf and hearing individuals were solely dueto lack of auditory experience, but that the combination of signlanguage usage and deafness may have had a large role in shapingthe cortical differences we observed.

THE CALCARINE SULCUS: SENSORY COMPENSATION ANDMULTISENSORY INTEGRATIONThere has been longstanding interest in the question of whetheror not compensatory visual enhancement accompanies congenitaldeafness (Bavelier et al., 2006). We examined the cortex surround-ing the calcarine sulcus (as a proxy for BA17, the primary visualcortex) to determine whether there was evidence of anatomicalchanges in deaf compared to hearing individuals. We had twomajor findings concerning the volume of the cortex surroundingthe calcarine sulcus. First, for all three participant groups, theright calcarine cortex volume was larger than the left; this patternwas indicated both by AI scores and pair-wise t-tests. A rightwardgray matter asymmetry in the cortex of the medial occipital lobein the neighborhood of the calcarine sulcus has been observedin several studies using automated assessment methods (VBM orcortical thickness; Good et al., 2001; Hervé et al., 2006; Luderset al., 2006; Takao et al., 2011; although see Watkins et al., 2001).Our results confirm these findings and provide a volumetric per-spective on this asymmetry in native-space (i.e., non-transformed)brain images. Consistent with our results and some of the VBMstudies, a direct histological volumetric assessment of the striatecortex has also shown that the right side is significantly larger thanthe left (Murphy, 1985). A rightward asymmetry of the striatecortex is consistent with the notion that visuo-spatial function ismore related to right hemisphere function (Corballis, 2003).

We also found evidence of increased total volume of the cal-carine cortex in the deaf group compared to the two hearinggroups (see Figure 2). Given the positive correlation between

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intracalcarine striate cortex volume and total striate cortex volume(Gilissen and Zilles, 1996), our findings suggest that deaf individ-uals on average may have more primary visual cortex than hearingindividuals (although such a conclusion would require histologicalverification). One study using VBM has shown increased size in thevisual cortex of deaf compared to hearing subjects, especially onthe right side (Leporé et al., 2010b). The increase was interpretedas evidence of possible sensory compensation for the absence ofauditory input. In contrast, Pénicaud et al. (2012) found reducedgray matter density in visual cortex for deaf individuals, but onlyfor those who learned sign language as a first language late inchildhood. Pénicaud et al. (2012, p. 7) reported increased densityfor deaf native signers (compared to hearing non-signers), andthey hypothesized that early ASL acquisition is associated withthe increase in gray matter density, which may arise because of“greater computational power in the visual cortex leading to amore efficient visual-perceptual analysis of the sign language sig-nal.” However, given that native hearing signers in our study didnot differ significantly from hearing non-signers, our findings sug-gest that it may be the combination of auditory deprivation andexposure to ASL in infancy that leads to a significant increase ingray matter volume within the calcarine cortex.

If increased size of the visual cortex in deaf individuals is atleast in part a result of visual compensation for deafness, therecould be evidence of altered visual abilities in deaf comparedto hearing individuals. Although a fair amount of research hasaddressed these questions, deaf individuals do not seem to per-form all that differently from hearing individuals on a range ofvisual-perceptual threshold tasks, such as coherent motion orflicker-fusion thresholds (for reviews, see Bavelier et al., 2006;Pavani and Bottari, 2012). However, several studies have shownthat deaf individuals are significantly faster to detect abrupt visualonsets (e.g., Loke and Song, 1991; Reynolds, 1993), and Bottariet al. (2011) recently showed that this ability is correlated with ERPcomponents in striate cortex (the C1 component, 80 ms from stim-ulus onset). The increased cortical volume found in the calcarinesulcus for deaf individuals might be related to this enhanced abil-ity to rapidly react to visual stimuli. In addition, the most robustdifferences between deaf and hearing people are seen on tests thatdepend on peripheral vision. Deaf individuals have a significantadvantage in attending to peripheral stimuli, which results in arelatively expanded FOV (Dye et al., 2009). One manifestation ofthis finding is that deaf individuals are more influenced by periph-eral distractors than central distractors, the opposite of the patternobserved for hearing individuals (Proksch and Bavelier, 2002). Indeaf individuals the increased peripheral sensitivity is correlatedwith an increase in the area of the neural rim of the retina, sug-gesting that the advantage is in fact due to early sensory changes(Codina et al., 2011). Thus it is possible that the expanded calcarinecortex in deaf individuals is also related to expanded attention tothe periphery of the visual field.

In addition to a compensatory model for the possible expansionof striate cortex in deaf signers, the dynamic nature of neuronaland synaptic plasticity that occurs in the context of auditoryand visual convergence, or multisensory activation (Bavelier andHirshorn, 2010) may also contribute to anatomical changes. Inte-gration between primary visual and auditory cortices is pervasive,

at both the structural and functional levels (Kayser and Logo-thetis, 2007; Raij et al., 2010). Cortical plasticity is thus very mucha function of dynamic interactions within neural networks, andthe changes in the calcarine that we observed may be a result ofboth visual compensation for auditory deprivation and changes inmultisensory integration networks. Further research is needed toclarify the potential contributions of each of these factors in shap-ing the structural and functional anatomy of the deaf primaryvisual cortex.

PARS TRIANGULARIS AND PARS OPERCULARIS: EFFECTS OFDEAFNESS ON LANGUAGE-RELATED CORTICESOur results revealed that the pars triangularis (bilaterally and com-bined) was significantly larger in the deaf group compared to eitherof the hearing groups. The pars opercularis showed no significantgroup differences, although there was a trend for larger volumesin the deaf group. These results partially replicate the findings ofLeporé et al. (2010b). Given that our finding pertains only to thedeaf group, it suggests that the increased volume in the pars tri-angularis is associated with deafness, rather than with life-longsigning. The IFG (pars triangularis and opercularis) is known tobe involved in a variety of linguistic and cognitive functions thatmay differ for deaf and hearing individuals (e.g., text reading,speech production and comprehension, working memory, humanaction recognition, etc.). However, we speculate that the increaseddemands faced by congenitally deaf individuals for decipheringspoken language through both print and lip reading may underliethe increased cortical volumes observed here.

For deaf children, access to sound-based phonology is greatlyreduced or absent, and many struggle to learn to read. Recentneuroimaging studies with deaf adults have reported that whenthe reading task requires phonological processing, deaf readersexhibit greater activation in the IFG (both pars triangularis andpars opercularis) compared to hearing readers (Aparicio et al.,2007; Emmorey et al., 2013b). Less skilled deaf readers also showgreater right inferior frontal activation in an implicit reading taskcompared to more skilled deaf readers (Corina et al., 2012). Fur-thermore, MacSweeney et al. (2009) found that adult deaf readersand hearing dyslexic individuals showed increased activation ofthe left IFG during a phonological rhyming judgment (comparedto hearing normal readers). Phonological processing is disruptedin both deaf and dyslexic individuals (for different reasons), andincreased activation in left IFG appears to arise as a compensatorymechanism during phonological tasks. Thus, it is possible that thedemands of learning to read a language that one cannot hear exactsmore intense processing in core association areas, including boththe left and right inferior frontal gyri, leading to their increase insize.

In addition, the demands of acquiring spoken language primar-ily from visual input may also lead to an increase in the volumeof the pars triangularis. For deaf individuals, speech reading willhave to rely, necessarily, on visual and articulatory rather thanauditory cues. The increased volume of Broca’s area (mainly parstriangularis) shown here, and the increased volume of the left pos-terior insula described earlier (Allen et al., 2008a), may representevidence for a speech reading network in deaf individuals linkinglanguage processing and multisensory integration.

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SIGN LANGUAGE AND MOTOR HANDKNOB ASYMMETRYThe handknob is a reliable landmark for the position of the handprimary motor cortex in the precentral gyrus (M1; Yousry et al.,1997; Sastre-Janer et al., 1998). However, the anatomy of the hand-knob displays considerable inter-individual variation, which maymake it difficult to detect structuro-functional changes that mightarise due to activity or experience (Caulo et al., 2007; Boling et al.,2008).

Surprisingly, an expected direct link between anatomy (thevolume or gray matter density of the handknob) and handed-ness has not been definitively established. The strong expectationis that the handknob would be larger on the contralateral sideto the dominant hand. Direct evidence to support or refute thisexpectation has been lacking, possibly because there have beenvery few direct volumetric studies of the human handknob, andvarious proxy or indirect measurements have produced equivocalresults (see Amunts et al., 1996 vs. Davatzikos and Bryan, 2002).An automated analysis of global patterns of cortical thickness inthe cerebrum shows a leftward asymmetry in the superior portionof the precentral gyrus, a region that would include the hand-knob (Luders et al., 2006). In contrast, a VBM study using a ROIapproach, showed greater gray matter density in a region aroundthe central sulcus near the location of the handknob in the righthemisphere of both left- and right-handers (Hervé et al., 2005).Histological studies have shown that BA 4 volume (the whole ofthe primary motor cortex including the hand region) is essen-tially symmetrical in right-handers, with no laterality evident inthe region corresponding to the handknob (White et al., 1997;Rademacher et al., 2001). Of course, these studies are measuringdifferent aspects of the motor region, and doing so using quitedifferent methods, although they all exhibit a potential relation tothe motor hand cortex.

Our results for right-handed non-signers, based on directanatomical measurement of the volume of gray matter encom-passed by the region corresponding to the hand, are consistentwith those studies finding a rightward asymmetry in the hand-knob. Our AI indicated that the right hemisphere handknobwas about 14% larger than the left, a magnitude of asymmetrythat is generally considered to be noteworthy. It is interestingto note that neither of the two signing groups exhibited such arightward asymmetry: the hearing signers were essentially sym-metrical, while the deaf signers were actually 11% larger in theleft hemisphere. The AI of the deaf individuals was significantlydifferent from that of the hearing non-signers. This intrigu-ing finding together with the finding of essential symmetry in

the hearing signers suggests the possibility of activity-dependentplasticity resulting from sign language usage and deserves furtherinvestigation.

Our results are also consistent with Penhune et al.’s (2003)hypothesis that the fine motor control of the hands required forsigning leads to structural changes in the hand motor region. Fur-thermore, plastic gray matter changes in the hand region withmotor training have been reported (Granert et al., 2011). Thereare also reports of relative volumetric preservation of the vol-ume of the cortex in the hand regions in aging (both motorand sensory) in the hemisphere contralateral to the dominanthand (Bonilha et al., 2009). These findings support the possi-bility that the volume of the cortex of the hand region may bemaintained by activity. The possible increase of the left hand-knob cortex in native signers, the language dominant hemisphere,may be indicative not just of differences in motor activity butof the recruitment of this region into a primary language net-work when signing begins during an early critical period ofdevelopment.

CONCLUSIONCongenitally deaf individuals who are native users of sign lan-guage showed evidence of structural cortical changes in each ofthe three brain regions examined. Increased bilateral volumes ofthe calcarine cortex and the pars triangularis in deaf individualsrelative to the volumes of both signing and non-signing hear-ing individuals provide evidence of likely developmental corticalplasticity in response to an environment of auditory deprivation.Differences in lateralization of the motor hand region observedfor deaf and hearing signers may be related to early and pro-longed use of sign language. Because of the variability seen inthis region, this finding should be further pursued in larger sam-ples. Overall, the study of structural and functional brain anatomyin congenitally deaf signers provides an insight into the variety offorces that influence cognitive and structural adaptation to specificenvironments.

ACKNOWLEDGMENTSThis work was supported by grants from the National Insti-tute on Deafness and Other Communication Disorders (R01DC006708 and R01 DC010997), from the National Institute onChild Health and Human Development (R01 HD047736), andfrom the National Institute of Neurological Disorders and Stroke(NS 19632). Thanks to Jocelyn Cole for help in processing imagingdata.

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Conflict of Interest Statement: Theauthors declare that the research wasconducted in the absence of any com-mercial or financial relationships thatcould be construed as a potential con-flict of interest.

Received: 04 May 2013; paper pendingpublished: 31 May 2013; accepted: 19July 2013; published online: 02 August2013.Citation: Allen JS, Emmorey K, Bruss Jand Damasio H (2013) Neuroanatomicaldifferences in visual, motor, and lan-guage cortices between congenitally deafsigners, hearing signers, and hearing non-signers. Front. Neuroanat. 7:26. doi:10.3389/fnana.2013.00026Copyright: © 2013 Allen, Emmorey, Brussand Damasio. This is an open-access arti-cle distributed under the terms of theCreative Commons Attribution License(CC BY). The use, distribution or repro-duction in other forums is permitted,provided the original author(s) or licensorare credited and that the original publica-tion in this journal is cited, in accordancewith accepted academic practice. No use,distribution or reproduction is permit-ted which does not comply with theseterms.

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